Hypoxia induces PGC-1α expression and mitochondrial biogenesis in the myocardium of TOF patients
Abstract
PGC-1alpha, a potent transcriptional coactivator, is the major regulator of mitochondrial biogenesis and activity in the cardiac muscle. The dysregulation of PGC-1alpha and its target genes has been reported to be associated with congenital and acquired heart diseases. By examining myocardium samples from patients with Tetralogy of Fallot, we show here that PGC-1alpha expression levels are markedly increased in patients compared with healthy controls and positively correlated with the severity of cyanosis. Furthermore, hypoxia significantly induced the expression of PGC-1alpha and mitochondrial biogenesis in cultured cardiac myocytes. Mechanistic studies suggest that hypoxia-induced PGC-1alpha expression is regulated through the AMPK signaling pathway. Together, our data indicate that hypoxia can stimulate the expression of PGC-1alpha and mitochondrial biogenesis in the cardiac myocytes, and this process might provide a potential adaptive mechanism for cardiac myocytes to increase ATP output and minimize hypoxic damage to the heart.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Under chronic hypoxia, PGC1α is upregulated, resulting in a subsequent increase of mitochondrial biogenesis.
“Under chronic hypoxia, PGC1α is upregulated, resulting in a subsequent increase of mitochondrial biogenesis [175].”
From AMPK, Mitochondrial Function, and Cardiovascular Disease (2020) · cites this paper as [175]
Cites
Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R. C., et al. (1999) · Cell · doi:10.1016/s0092-8674(00)80611-x · Cited by 4,139 · see citing works
Self-citationA Cold-Inducible Coactivator of Nuclear Receptors Linked to Adaptive Thermogenesis
Puigserver, P., Wu, Z., Park, C. W., Graves, R., Wright, M., & Spiegelman, B. M. (1998) · Cell · doi:10.1016/s0092-8674(00)81410-5 · Cited by 3,864 · see citing works
Transcriptional co-activator PGC-1α drives the formation of slow-twitch muscle fibres
Lin, J., Wu, H., Tarr, P. T., Zhang, C.-Y., Wu, Z., Boss, O., Michael, L. F., Puigserver, P., Isotani, E., Olson, E. N., et al. (2002) · Nature · doi:10.1038/nature00904 · Cited by 2,546 · see citing works
Self-citationMetabolic control through the PGC-1 family of transcription coactivators
Lin, J., Handschin, C., & Spiegelman, B. M. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.05.004 · Cited by 2,130 · see citing works
Puigserver, P., & Spiegelman, B. M. (2003) · Endocrine Reviews · doi:10.1210/er.2002-0012 · Cited by 2,076 · see citing works
Peroxisome proliferator–activated receptor γ coactivator-1 promotes cardiac mitochondrial biogenesis
Lehman, J. J., Barger, P. M., Kovacs, A., Saffitz, J. E., Medeiros, D. M., & Kelly, D. P. (2000) · Journal of Clinical Investigation · doi:10.1172/jci10268 · Cited by 1,285 · see citing works
HIF-1 Regulates Cytochrome Oxidase Subunits to Optimize Efficiency of Respiration in Hypoxic Cells
Fukuda, R., Zhang, H., Kim, J.-W., Shimoda, L., Dang, C. V., & Semenza, G. L. (2007) · Cell · doi:10.1016/j.cell.2007.01.047 · Cited by 1,225 · see citing works
HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1α
Arany, Z., Foo, S.-Y., Ma, Y., Ruas, J. L., Bommi-Reddy, A., Girnun, G., Cooper, M., Laznik, D., Chinsomboon, J., Rangwala, S. M., et al. (2008) · Nature · doi:10.1038/nature06613 · Cited by 1,054 · see citing works
Arany, Z., He, H., Lin, J., Hoyer, K., Handschin, C., Toka, O., Ahmad, F., Matsui, T., Chin, S., Wu, P.-H., et al. (2005) · Cell Metabolism · doi:10.1016/j.cmet.2005.03.002 · Cited by 694 · see citing works
Mitochondrial energy metabolism in heart failure: a question of balance
Huss, J. M., & Kelly, D. P. (2005) · Journal of Clinical Investigation · doi:10.1172/jci24405 · Cited by 533 · see citing works
Hawley, S. A., Selbert, M. A., Goldstein, E. G., Edelman, A. M., Carling, D., & Hardie, D. G. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.45.27186 · Cited by 441 · see citing works
AMPK activation increases fatty acid oxidation in skeletal muscle by activating PPARα and PGC-1
Lee, W. J., Kim, M., Park, H. S., Kim, H. S., Jeon, M. J., Oh, K. S., Koh, E. H., Won, J. C., Kim, M., Oh, G. T., et al. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.12.011 · Cited by 420 · see citing works
Russell, L. K., Mansfield, C. M., Lehman, J. J., Kovacs, A., Courtois, M., Saffitz, J. E., Medeiros, D. M., Valencik, M. L., McDonald, J. A., & Kelly, D. P. (2004) · Circulation Research · doi:10.1161/01.res.0000117088.36577.eb · Cited by 402 · see citing works
AMP-Activated Protein Kinase in the Heart
Arad, M., Seidman, C. E., & Seidman, J. G. (2007) · Circulation Research · doi:10.1161/01.res.0000258446.23525.37 · Cited by 356 · see citing works
Finck, B. N., & Kelly, D. P. (2007) · Circulation · doi:10.1161/circulationaha.107.670588 · Cited by 281 · see citing works
Effects of α‐AMPK knockout on exercise‐induced gene activation in mouse skeletal muscle
Jørgensen, S. B., Wojtaszewski, J. F. P., Viollet, B., Andreelli, F., Birk, J. B., Hellsten, Y., Schjerling, P., Vaulont, S., Neufer, P. D., Richter, E. A., et al. (2005) · The FASEB Journal · doi:10.1096/fj.04-3144fje · Cited by 274 · see citing works
Lehman, J. J., & Kelly, D. P. (2002) · Clinical and Experimental Pharmacology and Physiology · doi:10.1046/j.1440-1681.2002.03655.x · Cited by 257 · see citing works
Sano, M., Abdellatif, M., Oh, H., Xie, M., Bagella, L., Giordano, A., Michael, L. H., DeMayo, F. J., & Schneider, M. D. (2002) · Nature Medicine · doi:10.1038/nm778 · Cited by 236 · see citing works
Rapidly Increased Neuronal Mitochondrial Biogenesis After Hypoxic-Ischemic Brain Injury
Yin, W., Signore, A. P., Iwai, M., Cao, G., Gao, Y., & Chen, J. (2008) · Stroke · doi:10.1161/strokeaha.108.520114 · Cited by 229 · see citing works
Gutsaeva, D. R., Carraway, M. S., Suliman, H. B., It, D., Shitara, H., Yonekawa, H., & Piantadosi, C. A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5654-07.2008 · Cited by 200 · see citing works
Mannella, C. A., Marko, M., Penczek, P. A., Barnard, D., & Frank, J. (1994) · Microscopy Research and Technique · doi:10.1002/jemt.1070270403 · Cited by 184 · see citing works
Huss, J. M., Levy, F. H., & Kelly, D. P. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m100277200 · Cited by 174 · see citing works
The Role of Mitochondria in Ischemic Heart Disease
Ferrari, R. (1996) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-199600003-00002 · Cited by 164 · see citing works
Sex-specific pathways in early cardiac response to pressure overload in mice
Witt, H., Schubert, C., Jaekel, J., Fliegner, D., Penkalla, A., Tiemann, K., Stypmann, J., Roepcke, S., Brokat, S., Mahmoodzadeh, S., et al. (2008) · Journal of Molecular Medicine · doi:10.1007/s00109-008-0385-4 · Cited by 159 · see citing works
Gene expression profile of rat adipose tissue at the onset of high-fat-diet obesity
Li, J., Yu, X., Pan, W., & Unger, R. H. (2002) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00516.2001 · Cited by 153 · see citing works
Horman, S., Beauloye, C., Vertommen, D., Vanoverschelde, J., Hue, L., & Rider, M. H. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m302403200 · Cited by 121 · see citing works
Yang, J., & Holman, G. D. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m410213200 · Cited by 118 · see citing works
Konrad, D., Rudich, A., Bilan, P. J., Patel, N., Richardson, C., Witters, L. A., & Klip, A. (2005) · Diabetologia · doi:10.1007/s00125-005-1713-7 · Cited by 113 · see citing works
Chi, N. (2004) · Cardiovascular Research · doi:10.1016/j.cardiores.2003.11.033 · Cited by 106 · see citing works
PGC-1α induces apoptosis in human epithelial ovarian cancer cells through a PPARγ-dependent pathway
Zhang, Y., Ba, Y., Liu, C., Sun, G., Ding, L., Gao, S., Hao, J., Yu, Z., Zhang, J., Zen, K., et al. (2007) · Cell Research · doi:10.1038/cr.2007.11 · Cited by 101 · see citing works
Self-citationAge-related decline in mitochondrial DNA copy number in isolated human pancreatic islets
Cree, L. M., Patel, S. K., Pyle, A., Lynn, S., Turnbull, D. M., Chinnery, P. F., & Walker, M. (2008) · Diabetologia · doi:10.1007/s00125-008-1054-4 · Cited by 93 · see citing works
Increased expression of heat shock protein-70 protects A549 cells against hyperoxia
Wong, H. R., Menendez, I. Y., Ryan, M. A., Denenberg, A. G., & Wispé, J. R. (1998) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.1998.275.4.l836 · Cited by 81 · see citing works
Wong, L. B., Park, C. L., & Yeates, D. B. (1998) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1998.275.2.c440 · Cited by 76 · see citing works
An Intrinsic Timer That Controls Cell-Cycle Withdrawal in Cultured Cardiac Myocytes
Burton, P. B. J., RAFF, M. C., Kerr, P., Yacoub, M. H., & Barton, P. J. R. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9524 · Cited by 74 · see citing works
Pathophysiology of Congenital Heart Disease in the Adult
Sommer, R. J., Hijazi, Z. M., & Rhodes, J. F. (2008) · Circulation · doi:10.1161/circulationaha.107.714428 · Cited by 71 · see citing works
Disch, D. L., Rader, T. A., Cresci, S., Leone, T. C., Barger, P. M., Vega, R., Wood, P. A., & Kelly, D. P. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.8.4043 · Cited by 70 · see citing works
Zhu, L., Sun, G., Zhang, H., Zhang, Y., Chen, X., Jiang, X., Jiang, X., Krauss, S., Zhang, J., Xiang, Y., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004182 · Cited by 61 · see citing works
Self-citationMitochondria and heart disease.
DiMauro, S., & Hirano, M. (1998) · PubMed · Cited by 50 · see citing works
Development of a Double-Chambered Right Ventricle After Repair of Tetralogy of Fallot
Moran, A. M., Hornberger, L. K., Jonas, R. A., & Keane, J. F. (1998) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(98)00034-5 · Cited by 48 · see citing works
Chen, W., Chen, H., Yu, S., Huang, C., Wang, T., Chen, J. J. W., Chien, C., Chen, H., Yang, P., & Lee, Y. (2005) · Shock · doi:10.1097/01.shk.0000170352.72694.36 · Cited by 42 · see citing works
Failure of Right Ventricular Adaptation in Children With Tetralogy of Fallot
Reddy, S., Osorio, J. C., Duque, A. M., Kaufman, B. D., Phillips, A. B. M., Chen, J. M., Quaegebeur, J. M., Mosca, R. S., & Mital, S. R. (2006) · Circulation · doi:10.1161/circulationaha.105.001248 · Cited by 38 · see citing works
PGC-1α Inhibits Oleic Acid Induced Proliferation and Migration of Rat Vascular Smooth Muscle Cells
Zhang, Y., Liu, C., Zhu, L., Jiang, X., Chen, X., Qi, X., Liang, X., Jin, S., Zhang, P., Li, Q., et al. (2007) · PLoS ONE · doi:10.1371/journal.pone.0001137 · Cited by 36 · see citing works
Self-citationYang, X., Freeman, L. J., & Ross, C. (2005) · Postgraduate Medical Journal · doi:10.1136/pgmj.2004.020172 · Cited by 35 · see citing works
Lebrecht, D., Kirschner, J., Geist, A., Haberstroh, J., & Walker, U. A. (2009) · Cardiovascular Pathology · doi:10.1016/j.carpath.2009.06.006 · Cited by 34 · see citing works
Moreno, A. J., Santos, D. L., & Palmeira, C. M. (1998) · PubMed · Cited by 17 · see citing works
Impairment of mitochondrial respiratory chain enzyme activities in tetralogy of fallot
Shinde, S., Save, V. C., Patil, N. D., Mishra, K. P., & Tendolkar, A. G. (2006) · Clinica Chimica Acta · doi:10.1016/j.cca.2006.09.011 · Cited by 16 · see citing works
Prenatal sonographic diagnosis of tetralogy of fallot
Tongsong, T., Sittiwangkul, R., Chanprapaph, P., & Sirichotiyakul, S. (2005) · Journal of Clinical Ultrasound · doi:10.1002/jcu.20147 · Cited by 12 · see citing works
Ultrastractural alterations of right and left ventricular myocytes in tetralogy of fallot.
Isomura, T., Hisatomi, K., Inuzuka, H., Suzuki, S., Hayashida, N., Nishimi, M., MARUYAMA, H., KOGA, M., Kosuga, K., & Ohishi, K. (1990) · The Kurume Medical Journal · doi:10.2739/kurumemedj.37.177 · Cited by 7 · see citing works
Left ventricular ultrastructure in pulmonary stenosis and in tetralogy of Fallot
Toussaint, M., Planch�, C., Duboc, D., Pfister, A., Lage, C. D., & Gu�rin, F. (1987) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/bf00734511 · Cited by 6 · see citing works
Mitochondrial respiratory chain enzyme activities in tetralogy of Fallot
Maurer, I., & Zierz, S. (1994) · Clinical Investigation · doi:10.1007/bf00252828 · Cited by 6 · see citing works
Gd, K., Gf, S., Ba, K., Bm, K., & Ad, L. (1979) · PubMed · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
AMPK, Mitochondrial Function, and Cardiovascular Disease
Wu, S., & Zou, M.-H. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21144987 · Cited by 286 · see citing works
AMP-activated protein kinase regulation and biological actions in the heart
Zaha, V. G., & Young, L. H. (2012) · Circulation Research · doi:10.1161/circresaha.111.255505 · Cited by 279 · see citing works
S-Nitrosylation: An Emerging Paradigm of Redox Signaling
Fernando, V., Zheng, X., Walia, Y., Sharma, V., Letson, J., & Furuta, S. (2019) · Antioxidants · doi:10.3390/antiox8090404 · Cited by 211 · see citing works
Zhang, W., Ren, H., Xu, C., Zhu, C., Wu, H., Liu, D., Wang, J., Liu, L., Li, W., Ma, Q., et al. (2016) · eLife · doi:10.7554/elife.21407 · Cited by 211 · see citing works
Self-citationSirt1 promotes autophagy and inhibits apoptosis to protect cardiomyocytes from hypoxic stress
Luo, G.-P., Zhao, J., Zhu, Y. K., Zhu, Y., Chen, B., Ma, R., Tang, F., & Xiao, Y. (2019) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2019.4125 · Cited by 187 · see citing works
Yuan, Y., Huang, S., Wang, W., Wang, Y., Zhang, P., Zhu, C., Ding, G., Liu, B., Yang, T., & Zhang, A. (2012) · Kidney International · doi:10.1038/ki.2012.188 · Cited by 158 · see citing works
Morris, K. C., Lin, H. W., Thompson, J. W., & Pérez‐Pinzón, M. A. (2011) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2010.229 · Cited by 128 · see citing works
Hypoxia Activation of Mitophagy and Its Role in Disease Pathogenesis
Wu, H., & Chen, Q. (2014) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.6204 · Cited by 118 · see citing works
Diabetes Mellitus, Mitochondrial Dysfunction and Ca2+-Dependent Permeability Transition Pore
Belosludtsev, K. N., Belosludtseva, N. V., & Dubinin, M. V. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186559 · Cited by 122 · see citing works
Tseng, A. H.-H., Wu, L.-H., Shieh, S.-S., & Wang, D. L. (2014) · Biochemical Journal · doi:10.1042/bj20140213 · Cited by 114 · see citing works
Self-citationYuan, Y., Chen, Y., Zhang, P., Huang, S., Zhu, C., Ding, G., Liu, B., Yang, T., & Zhang, A. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.03.015 · Cited by 116 · see citing works
Lecarpentier, Y., CLAES, V. A., Duthoit, G., & Hébert, J. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00429 · Cited by 99 · see citing works
Targeting energy pathways in kidney disease: the roles of sirtuins, AMPK, and PGC1α
Clark, A. J., & Parikh, S. M. (2020) · Kidney International · doi:10.1016/j.kint.2020.09.037 · Cited by 93 · see citing works
Jiang, Z., Cowell, R. M., & Nakazawa, K. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00116 · Cited by 89 · see citing works
Rational construction of a reversible arylazo-based NIR probe for cycling hypoxia imaging in vivo
Zhang, Y., Zhao, W., Chen, Y., Yuan, H., Fang, H., Yao, S., Zhang, C., Xu, H., Li, N., Liu, Z., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-22855-0 · Cited by 88 · see citing works
Self-citationSun, L., Zhao, M., Yu, X., Wang, H., He, X., Liu, J., & Zang, W. (2012) · Journal of Cellular Physiology · doi:10.1002/jcp.24277 · Cited by 88 · see citing works
Nuamnaichati, N., Mangmool, S., Chattipakorn, N., & Parichatikanond, W. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.00805 · Cited by 81 · see citing works
The implications of mitochondrial DNA copy number regulation during embryogenesis
Carling, P. J., Cree, L. M., & Chinnery, P. F. (2011) · Mitochondrion · doi:10.1016/j.mito.2011.05.004 · Cited by 79 · see citing works
Zhang, H., Liu, B., Li, T., Zhu, Y. K., Luo, G.-P., Jiang, Y., Tang, F., Zhao, J., & Xiao, Y. (2017) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2017.3213 · Cited by 80 · see citing works
ROS homeostasis, a key determinant in liver ischemic-preconditioning
Priéto, I., & Monsalve, M. (2017) · Redox Biology · doi:10.1016/j.redox.2017.04.036 · Cited by 81 · see citing works
Zhao, Y., Zhu, S., Wang, H., Wang, L., Du, T., Ye, Z., Zhai, D., Zhu, Z. G., Tian, X., Lu, Z., et al. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.104381 · Cited by 71 · see citing works
Amplification of Mitochondrial Activity in the Healing Response Following Rotator Cuff Tendon Injury
Thankam, F. G., Chandra, I., Kovilam, A. N., Diaz, C., Volberding, B. T., Dilisio, M. F., Radwan, M. M., Gross, R. M., & Agrawal, D. K. (2018) · Scientific Reports · doi:10.1038/s41598-018-35391-7 · Cited by 64 · see citing works
S-Nitrosylation in Tumor Microenvironment
Sharma, V., Fernando, V., Letson, J., Walia, Y., Zheng, X., Fackelman, D., & Furuta, S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094600 · Cited by 58 · see citing works
Adipose HIF-1α causes obesity by suppressing brown adipose tissue thermogenesis
Jun, J. C., Devera, R., Unnikrishnan, D. C., Shin, M., Bevans‐Fonti, S., Yao, Q., Rathore, A., Younas, H., Halberg, N., Scherer, P. E., et al. (2016) · Journal of Molecular Medicine · doi:10.1007/s00109-016-1480-6 · Cited by 57 · see citing works
Hypoxia Signaling in Parkinson’s Disease: There Is Use in Asking “What HIF?”
Pinilla, L. L., Ugun‐Klusek, A., Rutella, S., & Girolamo, L. A. D. (2021) · Biology · doi:10.3390/biology10080723 · Cited by 49 · see citing works
Adaptive Cardiac Metabolism Under Chronic Hypoxia: Mechanism and Clinical Implications
Su, Z., Liu, Y., & Zhang, H. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.625524 · Cited by 49 · see citing works
Microtubule associated protein 4 phosphorylation leads to pathological cardiac remodeling in mice
Li, L., Zhang, Q., Zhang, X., Zhang, J., Wang, X., Ren, J. T., Jia, J., Zhang, D., Jiang, X., Zhang, J., et al. (2018) · EBioMedicine · doi:10.1016/j.ebiom.2018.10.017 · Cited by 42 · see citing works
Self-citationThe potential of herbal drugs to treat heart failure: The roles of Sirt1/AMPK
Zhang, T., Xu, L., Guo, X., Tao, H., Liu, Y., Liu, X., Zhang, Y., & Meng, X. (2023) · Journal of Pharmaceutical Analysis · doi:10.1016/j.jpha.2023.09.001 · Cited by 45 · see citing works
PATTNAIK, B. R., Bodas, M., Bhatraju, N. K., Ahmad, T., Pant, R., Guleria, R., Ghosh, B., & Agrawal, A. (2016) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2015.11.036 · Cited by 42 · see citing works
IHG-1 Promotes Mitochondrial Biogenesis by Stabilizing PGC-1α
Hickey, F. B., Corcoran, J. B., Docherty, N. G., Griffin, B., Bhreathnach, Ú., Furlong, F. M., Martin, F., Godson, C., & Murphy, M. (2011) · Journal of the American Society of Nephrology · doi:10.1681/asn.2010111154 · Cited by 40 · see citing works
Belosludtseva, N. V., Matveeva, L. A., & Belosludtsev, K. N. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242316833 · Cited by 39 · see citing works
Mitochondrial DNA Mutation, Diseases, and Nutrient-Regulated Mitophagy
Yang, X., Zhang, R., Nakahira, K., & Gu, Z. (2019) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-082018-124643 · Cited by 36 · see citing works
Self-citationIntegrated Control of Fatty Acid Metabolism in Heart Failure
Li, X., & Bi, X. (2023) · Metabolites · doi:10.3390/metabo13050615 · Cited by 33 · see citing works
Selvakumar, G. P., Iyer, S. S., Kempuraj, D., Raju, M., Thangavel, R., Saeed, D., Ahmed, M. E., Zahoor, H., Raikwar, S. P., Zaheer, S. A., et al. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-0882-6 · Cited by 33 · see citing works
Immunometabolic cross-talk in the inflamed heart
Marelli‐Berg, F. M., & Aksentijević, D. (2019) · Cell Stress · doi:10.15698/cst2019.08.194 · Cited by 34 · see citing works
Chiang, M., Cheng, Y., Lin, K., & Yen, C.-H. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.11.003 · Cited by 33 · see citing works
Wang, D., Zhang, J., Lu, Y., Luo, Q., & Zhu, L. X. (2016) · IUBMB Life · doi:10.1002/iub.1537 · Cited by 32 · see citing works
Self-citationZhang, X., Li, L., Zhang, Q., Wei, Q., Lin, J., Jia, J., Zhang, J., Yan, T., Lv, Y., Jiang, X., et al. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00191 · Cited by 28 · see citing works
Self-citationBruns, I., Sauer, B., Burger, M. C., Eriksson, J. A., Hofmann, U., Braun, Y., Harter, P. N., Luger, A., Ronellenfitsch, M. W., Steinbach, J. P., et al. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.006993 · Cited by 30 · see citing works
Xu, J., Wakai, M., Xiong, K., Yang, Y., Prabakaran, A., Wu, S. P., Ahrens, D., Molina‐Portela, M. D. P., Ni, M., Bai, Y., et al. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.115403 · Cited by 32 · see citing works
Ohuchi, H., Kawata, M., Uemura, H., Akagi, T., Yao, A., Senzaki, H., Kasahara, S., Ichikawa, H., Motoki, H., Syoda, M., et al. (2022) · Circulation Journal · doi:10.1253/circj.cj-22-0134 · Cited by 28 · see citing works
Ramjiawan, A., Bagchi, R. A., Blant, A., Albak, L., Cavasin, M. A., Horn, T. R., McKinsey, T. A., & Czubryt, M. P. (2013) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00262.2012 · Cited by 27 · see citing works
Veeranki, S., Givvimani, S., Pushpakumar, S. B., & Tyagi, S. C. (2014) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00003.2014 · Cited by 24 · see citing works
Repeated sprint exercise in hypoxia stimulates HIF-1-dependent gene expression in skeletal muscle
Nava, R. C., McKenna, Z. J., Fennel, Z. J., Berkemeier, Q., Ducharme, J. B., Magalhães, F. D. C., Amorim, F. T., & Mermier, C. M. (2022) · European Journal of Applied Physiology · doi:10.1007/s00421-022-04909-3 · Cited by 24 · see citing works
Rao, J., Li, J., Liu, Y., Lü, P., Sun, X., Sugumaran, P. K., & Zhu, D. (2012) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-012-1313-z · Cited by 23 · see citing works
Ravindran, S., & Kurian, G. A. (2019) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-019-09794-8 · Cited by 23 · see citing works
Nam, H. G. W., Kim, W., Yoo, D. Y., Choi, J. H., Won, M., Hwang, I. K., Jeong, J. H., Hwang, H. S., & Moon, S. M. (2013) · Neurological Research · doi:10.1179/1743132813y.0000000158 · Cited by 22 · see citing works
Chi, L., Wang, N., Yang, W., Wang, Q., Zhao, D., Sun, T., & Li, W. (2019) · Journal of Cardiovascular Translational Research · doi:10.1007/s12265-019-09886-1 · Cited by 22 · see citing works
Self-citationMitochondria in hypoxic pulmonary hypertension, roles and the potential targets
Geng, Y., Hu, Y., Zhang, F., Tuo, Y., Ge, R., & Bai, Z. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1239643 · Cited by 23 · see citing works
Druyan, S., & Levi, E. (2012) · Gene Expression Patterns · doi:10.1016/j.gep.2012.05.001 · Cited by 19 · see citing works
Sanz, M., Farine, E., Niederberger, P., Méndez‐Carmona, N., Wyss, R. K., Arnold, M., Gulac, P., Fiedler, M., Gressette, M., Garnier, A., et al. (2018) · American Journal of Transplantation · doi:10.1111/ajt.15024 · Cited by 19 · see citing works
Li, F., Guo, S., Wang, C., Huang, X., Wang, H., Tan, X., Cai, Q., Wu, J., Zhang, Y., Chen, X., et al. (2018) · BMC Complementary and Alternative Medicine · doi:10.1186/s12906-018-2319-1 · Cited by 19 · see citing works
Song, H., Polster, B. M., & Thompson, L. P. (2021) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00004.2021 · Cited by 18 · see citing works
Preobrazenski, N., Islam, H., & Gurd, B. J. (2021) · European Journal of Applied Physiology · doi:10.1007/s00421-021-04669-6 · Cited by 17 · see citing works
Disorders of gut microbiota in children with Tetralogy of Fallot
Liu, X., Lu, S., Shao, Y., Zhang, D., Tu, J., & Chen, J. (2022) · Translational Pediatrics · doi:10.21037/tp-22-33 · Cited by 17 · see citing works
Rodríguez‐Calvo, R., Vázquez‐Carrera, M., Masana, L., & Neumann, D. (2015) · PPAR Research · doi:10.1155/2015/785783 · Cited by 17 · see citing works
From metabolism to malignancy: the multifaceted role of PGC1α in cancer
Wang, Y., Peng, J., Yang, D., Xing, Z., Jiang, B., Xu, D., Jiang, C., Ouyang, B., & Su, L. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1383809 · Cited by 15 · see citing works
Histologic alterations in tetralogy of Fallot
Alpat, Ş., Yilmaz, M., Onder, S. C., Sargon, M. F., Güvener, M., Doğan, R., Demircin, M., & Paşaoğlu, İ. (2016) · Journal of Cardiac Surgery · doi:10.1111/jocs.12873 · Cited by 15 · see citing works
Tai, S., Fu, Y. H., Yang, Y., & Wang, J. J. (2015) · Transplantation Proceedings · doi:10.1016/j.transproceed.2014.11.057 · Cited by 12 · see citing works
Self-citationNatarajan, B., Arige, V., Khan, A. A., Reddy, S. S., Barthwal, M. K., Mahapatra, N. R., Barthwal, M. K., & Mahapatra, N. R. (2020) · Hypertension Research · doi:10.1038/s41440-020-00539-4 · Cited by 11 · see citing works
Han, Y., Xie, N., Cao, L., Zhao, X., Liu, X., Jiang, H., & Chi, Z. (2011) · Neuroscience Letters · doi:10.1016/j.neulet.2011.06.020 · Cited by 11 · see citing works
Grape Powder Improves Age‐Related Decline in Mitochondrial and Kidney Functions in Fischer 344 Rats
Pokkunuri, I. D., Ali, Q., & Asghar, M. (2016) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2016/6135319 · Cited by 11 · see citing works
Skeletal Muscle mRNA Response to Hypobaric and Normobaric Hypoxia After Normoxic Endurance Exercise
Ross, C. I., Shute, R. J., Ruby, B. C., & Slivka, D. R. (2019) · High Altitude Medicine & Biology · doi:10.1089/ham.2018.0147 · Cited by 11 · see citing works
Wang, M., Chen, J., Zhang, Z., Wang, T., Zhao, J., Wang, X., Wang, J., & Zhuang, H. (2025) · Nutrients · doi:10.3390/nu17172800 · Cited by 10 · see citing works
Self-citationRole of MOTS-c in the regulation of bone metabolism
Yi, X., Hu, G., Yang, Y., Li, J., Jin, J., & Chang, B. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1149120 · Cited by 10 · see citing works
Ren, C., Xi, L., Li, H., Pan, Z., Li, Y., Wang, G., Dai, J., He, D., Fan, S., & Wang, Q. (2024) · Life Sciences · doi:10.1016/j.lfs.2024.123084 · Cited by 10 · see citing works
Self-citationPivotal role of activating transcription factor 6α in myocardial adaptation to chronic hypoxia
Zhao, J., Li, J.-B., Ma, R., Chen, L., Wang, X., & Xiao, Y. (2012) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2012.03.004 · Cited by 10 · see citing works
Ngamsiri, P., Watcharasit, P., & Satayavivad, J. (2013) · Mitochondrion · doi:10.1016/j.mito.2013.11.003 · Cited by 10 · see citing works
Qin, J., Wang, Y., Tan, L., Yang, Y., Fu, Y., Wu, C., Duan, H., Li, C., Li, H., Zhou, S., et al. (2024) · Chemical Engineering Journal · doi:10.1016/j.cej.2024.158385 · Cited by 9 · see citing works
Liang, W., Wu, H., Long, Q., Lin, H. L., Lv, X., Ma, W., Wu, T., Ai, L., Zheng, Q., Guo, J., et al. (2025) · Life Sciences · doi:10.1016/j.lfs.2025.123564 · Cited by 9 · see citing works
Li, J., Zhang, Y., Liu, Y., Shen, T., Zhang, H., Xing, Y. T., & Zhu, D. (2014) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2014.10.015 · Cited by 9 · see citing works
Ji, S., Xu, X., Li, Y., Sun, S., Fu, Q., Qiu, Y., Wang, S., Xia, S., Wang, F., Zhang, F., et al. (2024) · Pharmaceuticals · doi:10.3390/ph17121727 · Cited by 8 · see citing works
Bahr, A. C., Naasani, L. I. S., de Gregório, E., Wink, M. R., Araújo, A. S. D. R., Türck, P., & Lago, P. D. (2024) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/j.jphotobiol.2024.112991 · Cited by 8 · see citing works
Xu, W., Hou, D., Jiang, X., Lu, Z., Guo, T., Liu, Y., Wang, D., Zen, K., Yu, B., & Zhang, C. (2011) · Journal of Cellular Physiology · doi:10.1002/jcp.24015 · Cited by 8 · see citing works
Self-citationGuo, L., & Gu, Z. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1207603 · Cited by 7 · see citing works
Self-citationElbatarny, M., Lu, Y. T., Hu, M., Coles, J. C., Mital, S. R., Ross‐White, A., Honjo, O., Barron, D. J., & Gramolini, A. O. (2025) · EBioMedicine · doi:10.1016/j.ebiom.2025.105839 · Cited by 7 · see citing works
Xie, W., Hong, Z., Xie, Y., Hou, K., Li, S., Fang, M., Guan, Y., Zhang, Z., & Zhang, M. (2025) · The FASEB Journal · doi:10.1096/fj.202501549rr · Cited by 5 · see citing works
Ferulic acid protects against stress-induced myocardial injury in mice
Li, S., He, P., Liu, J., Zang, S., Luo, J., Luo, Y., Zhu, S., & Zang, L. (2025) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2025.117309 · Cited by 5 · see citing works
Molecular alterations during female reproductive aging: Can aged oocytes remind youth?
Takahashi, Y. K. (2012) · InTech eBooks · doi:10.5772/35938 · Cited by 5 · see citing works
Dioxygen and Metabolism; Dangerous Liaisons in Cardiac Function and Disease
Angelini, A., Pi, X., & Xie, L. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.01044 · Cited by 6 · see citing works
Exploring mitochondrial dynamics and localization under cellular stress: A comprehensive insight
Agarwal, S., Karuppusamy, K. A., & Gupta, A. K. (2025) · Journal of Biosciences · doi:10.1007/s12038-025-00514-6 · Cited by 4 · see citing works
Kar, A., Gupta, S., Matilal, A., & Sarkar, S. (2025) · Nanomedicine · doi:10.1080/17435889.2025.2491989 · Cited by 4 · see citing works
Impact of Hypoxic Exercise Recovery on Skeletal Muscle Glycogen and Gene Expression
Slivka, D. R., Dumke, C. L., Hailes, W. S., & Ruby, B. C. (2021) · High Altitude Medicine & Biology · doi:10.1089/ham.2021.0028 · Cited by 4 · see citing works
Harley, G., & Mount, P. F. (2025) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/j.jpet.2025.103741 · Cited by 3 · see citing works
Warwick, A. M., Bomze, H. M., Wang, L., Hao, Y., Stinnett, S. S., & Gospe, S. M. (2024) · Scientific Reports · doi:10.1038/s41598-024-75916-x · Cited by 3 · see citing works
Cancer cachexia has many symptoms but only one cause: anoxia
Koltai, T. (2020) · F1000Research · doi:10.12688/f1000research.22624.1 · Cited by 3 · see citing works
Meta‐analysis reveals differential gene expression in tetralogy of Fallot versus controls
Voskamp, S., Hammonds, M., Knapp, T. M., Pekmezian, A. L., Hadley, D., & Nelson, J. S. (2023) · Birth Defects Research · doi:10.1002/bdr2.2293 · Cited by 3 · see citing works
Liu, S., Ding, R., Huang, L., Lv, J., Sun, Z., Wang, X., & Duan, J. (2025) · Journal of Advanced Research · doi:10.1016/j.jare.2025.05.041 · Cited by 2 · see citing works
PGC-1α-Derived Peptide Influences Energy in Normal Human Dermal Fibroblasts
Suchá, L., Šuláková, R., Fryčák, R., & Dolečková, I. (2018) · Cosmetics · doi:10.3390/cosmetics5010018 · Cited by 2 · see citing works
Zhang, Z., Zhao, Z., Luo, Z., Duan, X., Xiao, Y., Huang, J., Wang, Q., Liu, F., Ding, L., Gu, L., et al. (2026) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2026.03.009 · Cited by 1 · see citing works
Self-citationThe Role of Mitochondrial DNA in Tumorigenesis
Yeung, K. Y., Dickinson, A., & John, J. C. S. (2012) · Humana Press eBooks · doi:10.1007/978-1-62703-101-1_6
PGC-1 Alpha Levels in Muscle Fibers During Hind Limb Ischemia. 6 7
Veeranki, S., Givvimani, S., Pushpakumar, S. B., & Tyagi, S. C. (2014)
Iden, J. (2015) · ERA: Education and Research Archive (University of Alberta) · doi:10.7939/r3vd6pg31
Natarajan, B., Arige, V., Khan, A. A., Reddy, S. S., Santhoshkumar, R., Sagar, B. K. C., Barthwal, M. K., & Mahapatra, N. R. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/816470
Wood, A. J. (2021) · Scholarship@Western (Western University)
Increase in blood derived mitochondrial DNA copy number in strabismus patients
Zehra, Z., Zia, M. A., Siddiqui, S. N., von Bartheld, C. S., Azam, M., & Qamar, R. (2024) · Journal of American Association for Pediatric Ophthalmology and Strabismus · doi:10.1016/j.jaapos.2024.104042
Mitochondria in Pediatric Cardiovascular Diseases
Marı́n-Garcı́a, J. (2012) · Springer eBooks · doi:10.1007/978-1-4614-4599-9_12
PGC1α-mediated upregulation of PHD2 represses HIF-signaling, limiting prostate cancer progression
Fagoaga-Eugui, M., Martín-Martín, N., Zabala‐Letona, A., Iriondo, O., Talamillo, A., Valcárcel-Jiménez, L., Pérez-Andrés, E., Carlivaris, O., Garcia‐Longarte, S., Medina‐Jover, F., et al. (2026) · Cell Death and Differentiation · doi:10.1038/s41418-026-01858-8
- Authors
- Zhu, L., Wang, Q., Zhang, L., Fang, Z., Zhao, F., Lv, Z., Gu, Z., Zhang, J., Wang, J., Zen, K., Xiang, Y., Wang, D., & Zhang, C.-Y.
- Affiliations
- State Key Laboratory of Pharmaceutical Biotechnology (CN)
- Nanjing Drum Tower Hospital (CN)
- University of Toronto (CA)
- Corresponding author
- Wang, Jin
- Xiang, Yang
- Wang, Dongjin
- ORCID
- Venue
- Cell Research
- Published
- 2010-04-06
- Volume
- 20
- Issue
- 6
- Pages
- 676-687
- ISSN
- 1001-0602 (ISSN-L)
- 1748-7838
- OpenAlex
- W2153310447
- Cited by
- 101
- References
- 51
- Citations by year
- 2026: 2 · 2025: 10 · 2024: 7 · 2023: 7 · 2022: 3 · 2021: 8 · 2020: 7 · 2019: 9 · 2018: 7 · 2017: 3 · 2016: 7 · 2015: 3 · 2014: 6 · 2013: 5 · 2012: 12
- FWCI
- 2.86
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Cell Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Keywords
- PGC-1α, mitochondrial biogenesis, hypoxia, tetralogy of Fallot, congenital heart disease, cardiomyocytes, AMPK signaling, cyanosis, myocardium, myocardial energy metabolism
- MeSH terms
- Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha, Adolescent, Adult, Hypoxia, Cells, Cultured, Child, Child, Preschool, Female, Gene Expression Regulation, Heat-Shock Proteins, Humans, Infant, Male, Mitochondria, Myocardium, Tetralogy of Fallot, Transcription Factors, Signal Transduction, Biomarkers, Up-Regulation, Myocytes, Cardiac, AMP-Activated Protein Kinases, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review